Pavel Štys

OVARIOLE TYPES AND THE PHYLOGENY OF HEXAPODS

CONTENTS

The Complete Mitochondrial Genome and Novel Gene Arrangement of the Unique-Headed Bug Stenopirates sp. (Hemiptera: Enicocephalidae)

Many of true bugs are important insect pests to cultivated crops and some are important vectors of human diseases, but few cladistic analyses have addressed relationships among the seven infraorders of Heteroptera. The Enicocephalomorpha and Nepomorpha are consider the basal groups of Heteroptera, but the basal-most lineage remains unresolved. Here we report the mitochondrial genome of the unique-headed bug Stenopirates sp., the first mitochondrial genome sequenced from Enicocephalomorpha. The Stenopirates sp. mitochondrial genome is a typical circular DNA molecule of 15, 384 bp in length, and contains 37 genes and a large non-coding fragment. The gene order differs substantially from other known insect mitochondrial genomes, with rearrangements of both tRNA genes and protein-coding genes. The overall AT content (82.5%) of Stenopirates sp. is the highest among all the known heteropteran mitochondrial genomes. The strand bias is consistent with other true bugs with negative GC-skew and positive AT-skew for the J-strand. The heteropteran mitochondrial atp8 exhibits the highest evolutionary rate, whereas cox1 appears to have the lowest rate. Furthermore, a negative correlation was observed between the variation of nucleotide substitutions and the GC content of each protein-coding gene. A microsatellite was identified in the putative control region. Finally, phylogenetic reconstruction suggests that Enicocephalomorpha is the sister group to all the remaining Heteroptera.

Personality matters: individual variation in reactions of naive bird predators to aposematic prey.

Variation in reactions to aposematic prey is common among conspecific individuals of bird predators. It may result from different individual experience but it also exists among naive birds. This variation may possibly be explained by the effect of personality—a complex of correlated, heritable behavioural traits consistent across contexts. In the great tit (Parus major), two extreme personality types have been defined. ‘Fast’ explorers are bold, aggressive and routine-forming; ‘slow’ explorers are shy, non-aggressive and innovative. Influence of personality type on unlearned reaction to aposematic prey, rate of avoidance learning and memory were tested in naive, hand-reared great tits from two opposite lines selected for exploration (slow against fast). The birds were subjected to a sequence of trials in which they were offered aposematic adult firebugs (Pyrrhocoris apterus). Slow birds showed a greater degree of unlearned wariness and learned to avoid the firebugs faster than fast birds. Although birds of both personality types remembered their experience, slow birds were more cautious in the memory test. We conclude that not only different species but also populations of predators that differ in proportions of personality types may have different impacts on survival of aposematic insects under natural conditions.

The adipokinetic hormones of Heteroptera: a comparative study.

The adipokinetic hormones (AKHs) from 15 species of heteropteran Hemiptera (encompassing eight families, six superfamilies and three infraorders) have been isolated and structurally identified using liquid chromatography coupled with mass spectrometry. None of the structures are novel and all are octapeptides. These peptide sequence data are used, together with the previously available AKH sequence data on Heteroptera, to create a larger dataset for comparative analyses. This results, in total, in AKH sequences from 30 species (spanning 13 families), which are used in a matrix confronted with the current hypotheses on the phylogeny of Heteroptera. The expanded dataset shows that all heteropterans have octapeptide AKHs; three species have two AKHs, whereas the overwhelming majority have only one AKH. From a total of 11 different AKH peptides known from Heteroptera to date, three AKHs occur frequently: Panbo‐red pigment‐concentrating hormone (RPCH) (×10), Schgr‐AKH‐II (×6) and Anaim‐AKH (×4). The heteropteran database also suggests that particular AKH variants are family‐specific. The AKHs of Heteroptera: Pentatomomorpha (all terrestrial) are not present in Nepomorpha (aquatic) and Gerromorpha: Gerridae (semiaquatic); AKHs with a Val in position 2 are absent in the Pentatomomorpha (only AKHs with Leu2 are present), whereas Val2 predominates in the nonterrestrial species. An unexpected diversity of AKH sequences is found in Nepomorpha, Nepoidea, Nepidae and Nepinae, whereas Panbo‐RPCH (which has been identified in all infraorders of decapod crustaceans) is present in all analysed species of Pentatomidae and also in the only species of Tessaratomidae investigated. The molecular evolution of Heteroptera with respect to other insect groups and to crustaceans is discussed

Unusual organization of the tropharium in the telotrophic ovarioles of an insect, Saldula saltatoria

The tropharium of the common shorebug Saldula saltatoria consists of 2 zones: the apical mitotic region and the distal one comprising numerous mononucleate nurse cells. Each individual nurse cell is connected to the centrally located trophic core by a thin cytoplasmic projection referred to as a trophic process. The accumulations of a dense material interpreted as the remnants of intercellular bridge rim are observed associated with the trophic process membrane. In the light of these results the establishment of telotrophic ovarioles in hemipterans is discussed.

Phylogenetic divergences of the true bugs (Insecta: Hemiptera: Heteroptera), with emphasis on the aquatic lineages: the last piece of the aquatic insect jigsaw originated in the Late Permian/Early Triassic

Heteroptera are among the most diverse hemimetabolous insects. Seven infraorders have been recognized within this suborder of Hemiptera. Apart from the well‐established sister‐group relationship between Cimicomorpha and Pentatomomorpha (= Terheteroptera), the two terminal lineages, the relationships among the other five infraorders are still controversial, of which three (Gerromorpha, Nepomorpha and Leptopodomorpha) are intimately connected to aquatic environments. However, the various and often conflicting available phylogeny hypotheses do not offer a clear background for a connection between diversification and palaeoenvironments. In this study, a molecular data set representing 79 taxa and 10 149 homologous sites is used to infer the phylogenetic relationships within Heteroptera. Bayesian inference, maximum‐likelihood and maximum parsimony analyses were employed. The results of phylogenetic inferences largely confirm the widely accepted phylogenetic context. Estimation of the divergence time based on the phylogenetic results revealed that Gerromorpha, Nepomorpha and Leptopodomorpha originated successively during the period from the Late Permian to Early Triassic (269–246 Ma). This timescale is consistent with the origin and radiation time of various aquatic holometabolans. Our results indicate that the aquatic and semi‐aquatic true bugs evolved under environmental conditions of high air temperature and humidity in an evolutionary scenario similar to that of the aquatic holometabolans.

Organization of the tropharia in the telotrophic ovaries of the dipsocoromorphan bugs Cryptostemma alienum Herrich-Schaeffer and C. carpaticum Josifov (Heteroptera : Dipsocoridae)

Abstract The tropharia of the dipsocoromorphan bugs, Cryptostemma alienum and Cryptostemma carpaticum (Heteroptera : Dipsocoridae) are composed of 30–50 mononucleate nurse cells that are connected with centrally located trophic cores by means of broad cytoplasmic strands. The anteriormost nurse cells are markedly smaller and often reveal signs of degeneration. The trophic core is surrounded and penetrated by elaborate F-actin meshwork. Arrested oocytes and prefollicular cells are localized at the base of the tropharium. Anagenesis of heteropteran ovarioles is discussed in relation to the findings presented.

Adaptive change in protective coloration in adult striated shieldbugs Graphosoma lineatum (Heteroptera: Pentatomidae): test of detectability of two colour forms by avian predators

1. Protective coloration in insects may be aposematic or cryptic, and some species change defensive strategy between instars. In Sweden, the adult striated shieldbugs Graphosoma lineatum (Heteroptera: Pentatomidae) undergo a seasonal colour change from pale brown and black striation in the pre‐hibernating adults, to red and black striation in the same post‐hibernating individuals. To the human eye the pre‐hibernating adults appear cryptic against the withered late summer vegetation, whereas the red and black post‐hibernating adults appear aposematic. This suggests a possibility of a functional colour change. However, what is cryptic to the human eye is not necessarily cryptic to a potential predator.

Litter bugs exposed: phylogenetic relationships of Dipsocoromorpha (Hemiptera: Heteroptera) based on molecular data

Species in the heteropteran infraorder Dipsocoromorpha, or litter bugs, are small, cryptic, stunningly diverse and understudied. In addition to the vast amount of species discovery and morphological exploration that remain to be done in this group, phylogenetic relationships within the litter bugs are poorly understood. A phylogenetic framework will make Dipsocoromorpha more accessible for systematic studies at all levels and is therefore a first step towards a comprehensive treatment of the group. Using a molecular dataset (87 taxa of Hemiptera including 35 Dipsocoromorpha; two genes) and maximum likelihood and parsimony methods, we here aim to test, for the first time using cladistic methods and a comprehensive dataset, relationships within Dipsocoromorpha. We investigate if Dipsocoromorpha are monophyletic, shed light on the relationships among the three families included in this analysis, and study relationships within the largest family of Dipsocoromorpha, the Schizopteridae. Based on this dataset, we find that the monophyly of Dipsocoromorpha is strongly supported in all analyses and that Ceratocombidae and Dipsocoridae together are recovered as the sister group of Schizopteridae. Within Schizopteridae, Hypselosomatinae are treated as the sister group to a clade formed by the monophyletic Ogeriinae and monophyletic Schizopterinae. Within Schizopterinae, there is evidence for the monophyly of the Corixidea genus group, and we present additional infra-generic and genus-level hypotheses. We discuss these hypotheses in the light of current classifications and hypotheses on relationships and as the first contribution towards revealing the phylogenetic relationships of a remarkable and neglected clade of true bugs.

Scared by shiny? The value of iridescence in aposematic signalling of the hibiscus harlequin bug

Studies on aposematism have generally focused on the benefits of red or yellow coloration, occasionally in contrast with green or brown, but rarely blue or orange. Furthermore, almost no studies have explicitly studied the utility of iridescent coloration in aposematism. To evaluate the survival benefit of iridescent coloration, we tested the ability of the natural colour extremes of Tectocoris diophthalmus jewelbugs to induce initial avoidance, learned avoidance, discrimination from palatable alternatives and broad generalization against avian predators: naive hand-reared and experienced wild-caught great tits, Parus major. Artificial baits were created by hollowing out bugs and inserting pieces of mealworm. Preference tests presented iridescent and orange baits simultaneously, then birds were divided into training groups and sequentially exposed to palatable black baits alternated with iridescent or orange baits made unpalatable by soaking mealworms in quinine solution. This was followed by simultaneous black/coloured discrimination tests, then a generalization test with both previously experienced and novel baits (all palatable). All groups showed a preference for orange baits over ones with iridescent patches. For wild-caught birds, attack latencies of iridescent and orange training groups were statistically indistinguishable, although only orange caused increased attack latency over the sequence. Hand-reared birds showed no change in attack rate/latency towards iridescent bugs over the sequence. In postlearning discrimination tests, all groups showed equally strong preference for palatable black baits and their unpalatable training baits. In generalization tests, hand-reared birds were most averse towards trained baits, but increased avoidance of iridescent-and-black baits suggests iridescence alone can contribute to aposematism. Wild-caught birds showed strong aversion to iridescent and novel orange-and-black baits regardless of training, suggesting birds may be broadly generalizing experience from local red-and-black aposematic bugs. Results suggest iridescent coloration and patterning can be an effective aposematic signal, especially in the presence of alternative palatable prey and/or other aposematic species.